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1. Seasonal shifts in the gut microbiome indicate plastic responses to diet in wild geladas

   https://doi.org/10.1186/s40168-020-00977-9  

   Baniel, Alice ; Amato, Katherine R. ; Beehner, Jacinta C. ; Bergman, Thore J. ; Mercer, Arianne ; Perlman, Rachel F. ; Petrullo, Lauren ; Reitsema, Laurie ; Sams, Sierra ; Lu, Amy ; et al ( December 2021 , Microbiome)

   null (Ed.)

   Abstract Background Adaptive shifts in gut microbiome composition are one route by which animals adapt to seasonal changes in food availability and diet. However, outside of dietary shifts, other potential environmental drivers of gut microbial composition have rarely been investigated, particularly in organisms living in their natural environments. Results Here, we generated the largest wild nonhuman primate gut microbiome dataset to date to identify the environmental drivers of gut microbial diversity and function in 758 samples collected from wild Ethiopian geladas ( Theropithecus gelada ). Because geladas live in a cold, high-altitude environment and have a low-quality grass-based diet, they face extreme thermoregulatory and energetic constraints. We tested how proxies of food availability (rainfall) and thermoregulatory stress (temperature) predicted gut microbiome composition of geladas. The gelada gut microbiome composition covaried with rainfall and temperature in a pattern that suggests distinct responses to dietary and thermoregulatory challenges. Microbial changes were driven by differences in the main components of the diet across seasons: in rainier periods, the gut was dominated by cellulolytic/fermentative bacteria that specialized in digesting grass, while during dry periods the gut was dominated by bacteria that break down starches found in underground plant parts. Temperature had a comparatively smaller, but detectable, effect on the gut microbiome. During cold and dry periods, bacterial genes involved in energy, amino acid, and lipid metabolism increased, suggesting a stimulation of fermentation activity in the gut when thermoregulatory and nutritional stress co-occurred, and potentially helping geladas to maintain energy balance during challenging periods. Conclusion Together, these results shed light on the extent to which gut microbiota plasticity provides dietary and metabolic flexibility to the host, and might be a key factor to thriving in changing environments. On a longer evolutionary timescale, such metabolic flexibility provided by the gut microbiome may have also allowed members of Theropithecus to adopt a specialized diet, and colonize new high-altitude grassland habitats in East Africa. 

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2. Habitat fragmentation is associated with dietary shifts and microbiota variability in common vampire bats

   https://doi.org/10.1002/ece3.5228  

   Ingala, Melissa R. ; Becker, Daniel J. ; Bak Holm, Jacob ; Kristiansen, Karsten ; Simmons, Nancy B. ( May 2019 , Ecology and Evolution)

   Host ecological factors and external environmental factors are known to influence the structure of gut microbial communities, but few studies have examined the impacts of environmental changes on microbiotas in free‐ranging animals. Rapid land‐use change has the potential to shift gut microbial communities in wildlife through exposure to novel bacteria and/or by changing the availability or quality of local food resources. The consequences of such changes to host health and fitness remain unknown and may have important implications for pathogen spillover between humans and wildlife. To better understand the consequences of land‐use change on wildlife microbiotas, we analyzed long‐term dietary trends, gut microbiota composition, and innate immune function in common vampire bats (Desmodus rotundus) in two nearby sites in Belize that vary in landscape structure. We found that vampire bats living in a small forest fragment had more homogenous diets indicative of feeding on livestock and shifts in microbiota heterogeneity, but not overall composition, compared to those living in an intact forest reserve. We also found that irrespective of sampling site, vampire bats which consumed relatively more livestock showed shifts in some core bacteria compared with vampire bats which consumed relatively less livestock. The relative abundance of some core microbiota members was associated with innate immune function, suggesting that future research should consider the role of the host microbiota in immune defense and its relationship to zoonotic infection dynamics. We suggest that subsequent homogenization of diet and habitat loss through livestock rearing in the Neotropics may lead to disruption to the microbiota that could have downstream impacts on host immunity and cross‐species pathogen transmission.

    

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3. Characterization of captive and wild 13-lined ground squirrel cecal microbiotas using Illumina-based sequencing

   https://doi.org/10.1186/s42523-021-00154-9  

   Chiang, Edna ; Deblois, Courtney L. ; Carey, Hannah V. ; Suen, Garret ( January 2022 , Animal Microbiome)

   Hibernating animals experience extreme changes in diet that make them useful systems for understanding host-microbial symbioses. However, most of our current knowledge about the hibernator gut microbiota is derived from studies using captive animals. Given that there are substantial differences between captive and wild environments, conclusions drawn from studies with captive hibernators may not reflect the gut microbiota’s role in the physiology of wild animals. To address this, we used Illumina-based sequencing of the 16S rRNA gene to compare the bacterial cecal microbiotas of captive and wild 13-lined ground squirrels (TLGS) in the summer. As the first study to use Illumina-based technology to compare the microbiotas of an obligate rodent hibernator across the year, we also reported changes in captive TLGS microbiotas in summer, winter, and spring.

   Wild TLGS microbiotas had greater richness and phylogenetic diversity with less variation in beta diversity when compared to captive microbiotas. Taxa identified as core operational taxonomic units (OTUs) and found to significantly contribute to differences in beta diversity were primarily in the familiesLachnospiraceaeandRuminococcaceae. Captive TLGS microbiotas shared phyla and core OTUs across the year, but active season (summer and spring) microbiotas had different alpha and beta diversities than winter season microbiotas.

   This is the first study to compare the microbiotas of captive and wild rodent hibernators. Our findings suggest that data from captive and wild ground squirrels should be interpreted separately due to their distinct microbiotas. Additionally, as the first study to compare seasonal microbiotas of obligate rodent hibernators using Illumina-based 16S rRNA sequencing, we reported changes in captive TLGS microbiotas that are consistent with previous work. Taken together, this study provides foundational information for improving the reproducibility and experimental design of future hibernation microbiota studies.

    

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4. Seasonal Effects on the Fecal Microbial Composition of Wild Greater Thick-Tailed Galagos (Otolemur crassicaudatus)

   https://doi.org/10.1007/s10764-023-00407-1  

   Long, Channen ; Scheun, Juan ; Sauther, Michelle Linda ; Cuozzo, Frank P. ; Millette, James ; Tordiffe, Adrian Stephen ( November 2023 , International Journal of Primatology)

   Setchell, J (Ed.)

   Bacterial communities present in the host digestive tract are important for the breakdown and absorption of nutrients required by the host. Changes in diet and the environment are major factors affecting the composition and diversity of the fecal microbiome. In addition to changes in ambient temperature and rainfall, primates living in seasonal temperate environments also need to adapt to seasonal changes in food resource quantity and quality. However, there is a lack of information about the fecal microbiome in African strepsirrhines relative to other primate taxa. We examined the effects of seasonal dietary and environmental changes on fecal microbial alpha diversity and composition in wild greater thick-tailed galagos (Otolemur crassicaudatus) at Lajuma Research Centre, South Africa. We collected fecal samples and assessed food availability and weather in summer and winter across 1 year and used 16S rRNA next-generation sequencing to characterise the fecal microbiome of 49 animals. We found significant increases in rainfall, ambient temperature, and food availability in summer compared with winter. However, we found no significant changes in body mass or in the overall diversity of bacterial species present in fecal samples between the two seasons. We found significant decreases in the abundance of certain bacterial families in winter, suggesting a change in diet. Our findings suggest that greater thick-tailed galagos can find food resources to maintain their body mass throughout the year. Our insights into the seasonal fecal microbiome of greater thick-tailed galagos add to the growing knowledge and understanding of fecal microbiomes in primates and how they help primates cope with changes to their environments.

    

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5. Microbiome stability and structure is governed by host phylogeny over diet and geography in woodrats ( Neotoma spp.)

   https://doi.org/10.1073/pnas.2108787118  

   Weinstein, Sara B. ; Martínez-Mota, Rodolfo ; Stapleton, Tess E. ; Klure, Dylan M. ; Greenhalgh, Robert ; Orr, Teri J. ; Dale, Colin ; Kohl, Kevin D. ; Dearing, M. Denise ( November 2021 , Proceedings of the National Academy of Sciences)

   The microbiome is critical for host survival and fitness, but gaps remain in our understanding of how this symbiotic community is structured. Despite evidence that related hosts often harbor similar bacterial communities, it is unclear whether this pattern is due to genetic similarities between hosts or to common ecological selection pressures. Here, using herbivorous rodents in the genusNeotoma, we quantify how geography, diet, and host genetics, alongside neutral processes, influence microbiome structure and stability under natural and captive conditions. Using bacterial and plant metabarcoding, we first characterized dietary and microbiome compositions for animals from 25 populations, representing seven species from 19 sites across the southwestern United States. We then brought wild animals into captivity, reducing the influence of environmental variation. In nature, geography, diet, and phylogeny collectively explained ∼50% of observed microbiome variation. Diet and microbiome diversity were correlated, with different toxin-enriched diets selecting for distinct microbial symbionts. Although diet and geography influenced natural microbiome structure, the effects of host phylogeny were stronger for both wild and captive animals. In captivity, gut microbiomes were altered; however, responses were species specific, indicating again that host genetic background is the most significant predictor of microbiome composition and stability. In captivity, diet effects declined and the effects of host genetic similarity increased. By bridging a critical divide between studies in wild and captive animals, this work underscores the extent to which genetics shape microbiome structure and stability in closely related hosts.

    

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